Integrative and Comparative Biology Advance Access originally published online on May 5, 2006
Integrative and Comparative Biology 2006 46(4):368-372; doi:10.1093/icb/icj039
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Sexual selection in hermaphrodites: where did our ideas come from?
California Academy of Sciences 875 Howard Street, San Francisco, CA 94103, USA
Correspondence: 1E-mail: mghiselin{at}calacademy.org
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 Synopsis IntroductionHermaphroditismSexual selectionPutting hermaphroditism and...Reflections on the discoveryReferences |
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Interpretations of hermaphroditism have been influenced by the old idea that organisms can be arranged in a series from lower to higher, with human beings at the top, leading toward the angels and God (the scala naturae). The consequent notion that hermaphroditism is a primitive condition is still with us. Such issues need to be addressed empirically, in a phylogenetic context. Darwin's theory of sexual selection provided the key to understanding sex switches, but it was not invoked until 1969 when it was conjoined with ideas about relative size influenced by the work of Bernhard Rensch. In principle the problem could have been solved a century earlier, and genetics was misleading rather than helpful. What really helped was an appreciation of Darwin's nonteleological way of thinking.
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Introduction |
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SynopsisIntroductionHermaphroditismSexual selectionPutting hermaphroditism and...Reflections on the discoveryReferences |
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This article inevitably has substantial autobiographical content. After all, it was my paper entitled "The evolution of hermaphroditism among animals" (Ghiselin 1969a
) that first explained protandry and protogyny in terms of Darwin's theory of sexual selection. One of my goals is to explain, for the first time, how the "size advantage model" for sequential hermaphroditism came to be invented. That experience casts some light on the phenomena of creativity, something that has interested me literally since childhood. Because I am a serious intellectual historian as well as a zoologist, an insider's view can be related to some very interesting topics. Why, for example, was the discovery not made a century before? The basic answer is that Darwin's ideas ought to have been taken more seriously. |
Hermaphroditism |
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SynopsisIntroductionHermaphroditismSexual selectionPutting hermaphroditism and...Reflections on the discoveryReferences |
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The existence of hermaphroditic animals was known to the ancients, and human hermaphroditism was part of their mythology. The hermaphrodite was a symbol of, among other things, completeness. The notion, however, of having separate sexes (gonochorism) as the norm, and indeed the ideal, and hermaphroditism as somehow being a characteristic of the "lower" organisms has been widely presupposed down to the present day. The traditional notion of a scala naturae has it that man can be placed in a series from higher to lower, with God at the top, followed by the various ranks of angels, and with man at the head of a long series of animals, leading gradually downward to plants and unorganized matter. That kind of thinking was carried over into evolutionary biology and is particularly conspicuous in the works of Lamarck. Even Darwin (1871
, vol. 1, p 207), who replaced the ladder (scala) with a tree and invented genealogical classification, accepted the view of Gegenbaur (1870, p 876) that human beings are descended from remote hermaphroditic ancestors. Darwin had documented the evolution of separate sexes within one small group of barnacles, and that instance may have proved misleading.
Much of the credit for refuting the notion that hermaphroditism is primitive among animals should be given to the Belgian malacologist Paul Pelseneer (1894). A good systematist, with a genealogical outlook, he worked on a group, the gastropods, in which it is obvious that the more derived taxa (Opisthobranchia and their probable sister group Pulmonata) are the hermaphrodites. Establishing which it was that came first, the hermaphrodite or the gonochorist, is a little more difficult than showing that the egg preceded the chicken by hundreds of millions of years. But if we have data, we can show what happened. In surveying the literature on hermaphroditism in echinoderms, for example, I found it easy to show that it had evolved separately and repeatedly within the group, for the hermaphrodites occur scattered about in various taxa within the phylum. But we know that the transition can go both ways, and there are many open issues. There are opportunities for documenting what has happened using modern, up-to-date techniques. The point to be emphasized here is that historical questions need to be addressed using historical data and methods.
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Sexual selection |
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SynopsisIntroductionHermaphroditismSexual selectionPutting hermaphroditism and...Reflections on the discoveryReferences |
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Darwin's theory of sexual selection was one of his most brilliant accomplishments and perhaps the one that has been the least well understood. It is one of the best examples of Darwin's nonteleological way of thinking about adaptation—including maladaptation. Instead of asking what good things are, one asks what has been the history of reproductive competition within species. Darwin realized that in addition to natural selection, which depends upon relative use of environmental resources, there is selection that depends upon monopolizing the opportunities to contribute to the ancestry of the next generation. This was in addition to a third kind of selection, artificial selection, that depends upon decisions of the breeder and is more closely related to sexual, than to natural, selection. He speculated about what would happen if a pea-hen admired a peacock's tail as much as we do. And he realized that there is a nice analogy with ornamental poultry. Such phenomena as sexual dimorphism and male combat had been discussed by Darwin's predecessors, and their views have often been confused with his. The notion of eugenical selection, with stags fighting in order to improve the race, was a teleological idea that Darwin read about in the works of his paternal grandfather (Ghiselin 1976
). Darwin believed that female choice is the result of an aesthetic preference on the part of the females, and he did not consider it basically a matter of picking out "good genes." The discovery of Basolo (1990) that female preference for sexual ornaments existed before the ornaments themselves evolved came as a surprise in some quarters. It would hardly have surprised Darwin, for that was one of his basic hypotheses. He did think that more healthy organisms would win the contests, but that is not the same thing as the raison d'être of the competition itself. Of course he realized that natural selection and sexual selection interact in a complex manner. At present theorists are attempting to understand sexual selection in terms of tradeoffs that involve a certain amount of maladaptation, much as Darwin did (Wong and Candolin 2005). |
Putting hermaphroditism and sexual selection together |
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SynopsisIntroductionHermaphroditismSexual selectionPutting hermaphroditism and...Reflections on the discoveryReferences |
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Now I come in. After taking my undergraduate degree at the University of Utah, I went to Stanford and did my doctoral research under Donald P. Abbott at Hopkins Marine Station. My dissertation project was on the phylogeny of opisthobranch gastropods. These mollusks are simultaneous hermaphrodites with complex reproductive systems, and I was particularly interested in how the systems work. In January 1963 I purchased a copy of Evolution above the Species Level by Bernhard Rensch (1959)
. The book was particularly useful to me because Rensch dealt with the differences between large and small animals. That was important because I did not want to group organisms together simply because they are of the same size. Rensch, however, viewed such problems mainly in terms of physiological advantages, not reproductive competition. Late in the summer of 1963 I headed for the Indian Ocean, and on the way stopped at the Seto Marine Biological Laboratory of Kyoto University to do some research. There I met Jack Tomlinson who explained to me his ideas about the low density model, according to which animals that are male and female at the same time have less difficulty finding a suitable mate. Therefore I was aware of his ideas before they were published (Tomlinson 1966). When still in Japan I wrote a paper on a minute opisthobranch, Runcina setoensis, in which I explained the direct development of small gastropods on the basis of small clutch size making larval dispersal too risky (Ghiselin 1963). Evolutionary ecology was now beginning to enter into the thinking of a comparative functional anatomist.
While completing my dissertation I was much offended by the Stanford pheneticists, especially Paul Ehrlich and Michael Soulé, and soon thereafter helped to bring about the demise of that antiphylogenetic movement among systematists. During a postdoctoral year with Ernst Mayr at Harvard, I began serious work on the philosophy of systematics. The pheneticists advocated a kind of epistemology that is called "naïve inductionism." I, on the other hand, had been much impressed with the philosophy of Karl Popper and the hypothetico-deductive method, which involves serious attempts to refute hypotheses. To my knowledge the first explicit discussion of Popperian philosophy in relation to phylogenetics was a paper first drafted in late 1964 (Ghiselin 1966a). There were of course some later writings. Recently there has been some discussion (much of it unpublished) among historians, philosophers, and biologists as to where Popperian views entered into the discussion of the philosophy of systematics. One obvious link is my own publications, which were read by Mayr and his student, Walter Bock. The latter provoked the cladists into a debate that continues to the present.
Then, during my 2 years as a postdoctoral fellow at Woods Hole, I wrote a book on Darwin based on a careful reading of all of his major works. As a result of that project I came to understand Darwin's sexual selection theory very well, particularly from a philosophical point of view. While I was writing my book, George C. Williams's (1966) Adaptation and Natural Selection was published. It stressed the individualistic aspect of selection, which was salutary, but was rather simplistic about the hierarchy of individuals. My philosophical work at Harvard was particularly important in allowing me to understand the issues. For it was there that I came to develop the idea that species are individuals (Ghiselin 1966b), a thesis that later became the foundation of the theory of species selection (cf. Gould 2002) as well as the modern philosophy of systematics. Only some years later was I able to get the academic world to appreciate the individuality thesis (Ghiselin 1975). Williams himself obviously never understood it and dismissed it as a "fallacy" (Williams 1992: see Ghiselin 1997). I am not sure how much Williams's book helped me to understand Darwin, but it did help me to appreciate the extent to which species-level advantages had been invoked under circumstances where organismal advantages are more plausible. I began to see some possibilities for further research and became seriously interested in the relationship between species diversity and modes of reproduction.
Upon receiving the call to Berkeley in 1967, I began to work on the evolution of hermaphroditism. I realized that the low-density model would work for simultaneous hermaphrodites, but not for sequential ones. For better or for worse, I spent several weeks on a wild goose chase, for I was trying to develop Mayr's notion of a genetical environment, and operated within the "paradigm" of evolutionary synthesis. I invented a "gene dispersal model," which treated sequential hermaphroditism as a way of avoiding inbreeding. In trying to find relevant evidence, I read a great deal of literature. Then, one day in the old biology library I read a paper on a sex-switching fish. It remarked that the males are brightly colored. At once I realized that sexual selection might be operative and had a classic "aha" experience. It was not, however, a matter of the females choosing the more spectacular looking or aesthetically pleasing males, but rather of "male combat" with males fighting and the successful contestants monopolizing the opportunities to fertilize the eggs. The fish reproduced as females until they were big enough to win fights, and then turned into males. I had combined Darwin's ideas with those of Rensch. Thus was born the "size advantage model," which was published with a review of the literature as supporting material (Ghiselin 1969a). My book on Darwin was published the same year (Ghiselin 1969b). I do not know to what extent the correlation represents a cause–and-effect relationship, but shortly afterward sexual selection ceased to be virtually ignored by evolutionary biologists and it became generally recognized that, once again, Darwin had been right after all.
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Reflections on the discovery |
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SynopsisIntroductionHermaphroditismSexual selectionPutting hermaphroditism and...Reflections on the discoveryReferences |
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Several points about this discovery are of interest with respect to theories of scientific discovery and creativity.
To begin, the hypothesis was remarkably original. Not only has nobody ever challenged my priority for the size advantage model, but no real adumbrations of it have also thus far turned up in the publications of any other scientist. The closest I can come is in my own dissertation, in which I suggest that small pelagic gastropods might economize on space by first maturing as males (Ghiselin 1966c). Smith (1967) did suggest that age might play a factor. The sociologist Robert Merton (1973) argued that multiple discoveries rather than singletons are the general rule in science. This was definitely a singleton, though obviously others would sooner or later have come up with the same basic idea. Of course more is involved in making a discovery than coming up with a novel hypothesis. One has to know what to do with it and to convince the scientific community that it should be taken seriously.
That brings me to my second point, which is that the discovery was not contingent upon the discovery of new facts, concepts, or techniques. The theory of sexual selection was first mentioned in print in 1858, clearly explained in 1859, and vastly elaborated in 1871 (Darwin and Wallace 1858; Darwin 1859, 1871). Darwin was fully aware of the fact that male combat has sometimes led to the evolution of sexual dimorphism with respect to size. Hermaphrodites had been known to science since antiquity, and 19th century naturalists knew a great deal about them. Apparently it took about a 100 years before somebody framed the right question. It may seem odd that the size advantage model was discovered by a sea-slug genital anatomist. After all, any number of gastropod systematists had gathered data on reproductive characters before. However, my approach was more physiological than morphological and, unlike many systematists, I was seriously interested in evolutionary mechanisms and processes. My efforts to understand Rensch's ideas, and to apply them to my own research, made it much easier to think in terms of relative size in other contexts. New ideas do not come out of nowhere: they are rooted in earlier experience, though of course they also transcend it.
A third, and closely related, point is that not only was genetics unnecessary for making this discovery, but it was also somewhat of an impediment. My own experience in struggling with a conventional population-genetics hypothesis is only part of the point here. Our predecessors had become so obsessed with the gene that they failed to pay due attention to what really matters: the living organism and the conditions of existence. That, together with the importance of nonteleological thinking, was the basic point of my book on the economy of nature (Ghiselin 1974). Teleological thinking about genetics has given rise to such notions as selfish genes, which as I see it must include selfish chromosomal deletions (Ghiselin 2003). On top of that, a reductionist approach that even takes the metaphysical position that entities at higher levels are epiphenomena or do not even exist, diverts our attention from what is causally relevant. My point is not that genes are unimportant or uninteresting. Rather, it is that we should have a realistic conception of what they are and what they can tell us.
Fourth, Darwin had a profound grasp of evolutionary principles and mechanisms. It has always been easy to deal with evolution on a much more superficial level. The Synthetic theory, which was proclaimed victorious around 1950, was seriously tainted with teleology. The centennial of The Origin of Species in 1959 made it evident that the book itself should not be read as a mere historical curiosity. Likewise The Descent of Man, and Selection in Relation to Sex deserves to be read as a profound contribution to the philosophy of our subject. Understanding it that way certainly helped my own creativity. The take-home message here is that we often benefit from going back to fundamentals and giving them some serious thought.
And finally, the size advantage model provides an excellent example of a successful hypothesis. After more than 3 decades of research, it has never had a serious competitor and there is no reason for abandoning it. In other words, it is probably true. That makes it philosophically respectable to scientists, and maybe even to philosophers. No doubt it meets the Popperian criterion of being able to withstand efforts to refute it. On the other hand I called it a "model" and the term is apt because it can be varied so that age rather than size is what counts. Treating it as a model fits some alternative views of what science is all about. It also explains a great deal, and in a way that had not been anticipated. Explanatory value is a criterion for accepting hypotheses that seems to be more popular with scientists themselves than with philosophers. But I think that what has made the size advantage so attractive to scientists is the wonderful opportunities that it has opened up for us to do research. A brief overview will show what I mean and provide an opportunity to praise a few of my colleagues.
There are plenty of opportunities for doing field research, especially in pleasant places like coral reefs, with their sex-switching fishes. The pioneering work of Ross Robertson (1972) and Robert Warner (1975) provides outstanding examples. Sex switches can also be studied in the laboratory as we see in the work of Gabriella Sella (1988). Those who enjoy doing mathematics have made quite a number of valuable contributions (Warner and others 1975). These include theoreticians such as Eric Charnov (1982) who developed a very broad and general theory of sex allocation. Specialists on a wide variety of organisms, including plants, have been able to put their expertise to good use (Freeman and others 1980). For those of us who like to work in the library, there have been ample opportunities for compilation and synthesis. Hermaphroditism is an important topic in the multivolume work on marine invertebrate reproduction edited by Giese and Pearse (1974 and later volumes). Life has also been very good for those who enjoy speculating and enriching this area of research with new ideas, for example, Janet Leonard and Ken Lakowiak (1984). Finally, and this symposium could hardly provide a better illustration, we have a wonderful example of what can be accomplished when we take a broad, comparative approach to what is basically a natural history discipline.
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Acknowledgements |
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I am grateful to Nico Michiels and Janet Leonard for arranging for my participation at 2 meetings where versions of this article were presented and discussed, and also to both the anonymous referees of the manuscript.
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Footnotes |
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From the symposium "Sexual Selection and Mating Systems in Hermaphrodites" presented at the annual meeting of the Society for Integrative and Comparative Biology, January 4–8, 2005, at San Diego, California.
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References |
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SynopsisIntroductionHermaphroditismSexual selectionPutting hermaphroditism and...Reflections on the discoveryReferences |
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